PERSPECTIVE New perspectives on anthropoid origins Blythe A. Williamsa,1, Richard F. Kaya, and E. Christopher Kirkb aDepartment of Evolutionary Anthropology, Duke University, Durham, NC 27708-0383; and bDepartment of Anthropology, University of Texas, Austin, TX 78712 Edited by Alan Walker, Penn State University, University Park, PA, and approved January 19, 2010 (received for review September 22, 2009) Adaptive shifts associated with human origins are brought to light as we examine the human fossil record and study our own genome and that of our closest ape relatives. However, the more ancient roots of many human characteristics are revealed through the study of a broader array of living anthropoids and the increasingly dense fossil record of the earliest anthropoid radiations. Genomic data and fossils of early primates in Asia and Africa clarify relationships among the major clades of primates. Progress in comparative anatomy, genomics, and molecular biology point to key changes in sensory ecology and brain organization that ultimately set the stage for the emergence of the human lineage. primate | Haplorhini | Strepsirrhini | human evolution | phylogeny uman evolution did not begin primates (lemurs and lorises) is also well fossil record remains sparse and 6–8 million years ago with the supported by morphological and molecular incomplete. For decades, anthropoid H phylogenetic split between the evidence. However, the question of ancestors were sought in two taxonomically chimpanzee and human line- whether tarsiers are more closely related diverse radiations of primarily Eocene ages. Although the ape–human transition to anthropoids or strepsirrhines has been taxa: Omomyiformes and Adapiformes is of tremendous interest to specialists and less clear. Some classifications united (sometimes identified at the family or the general public, many key genetic tarsiers with strepsirrhines in the suborder superfamily level). Both groups are events and adaptive shifts leading to the Prosimii because they retain primitive common in North American and European origin of humans had already been set in features such as grooming claws and an Paleogene faunas and also occur in Africa motion long before this split. The seeds of unfused mandibular symphysis. An and Asia (5). Omomyiforms are fi fi these changes can be identi ed in the alternative phylogenetic classi cation considered haplorhines, and adapiforms earlier branches of the primate family tree, linked tarsiers with anthropoids in the strepsirrhines by most workers (6–8, but many millions of years in the past. semiorder Haplorhini. Evidence for a see ref. 9), although few characters Changes in sensory ecology, increases in haplorhine clade comes from an unambiguously support omomyiforms as brain size, and reorganization of the increasingly long list of derived hard and ’ haplorhine. The German adapiform brain s components set the stage for the soft tissue morphological features and from Darwinius was described as having features development of language and for many of molecular features. Molecular allying it, and by extension, other our other exceptional cognitive abilities. phylogenetic studies using DNA sequence adapiforms with Haplorhini (10). Recent well-publicized descriptions of data generally failed to provide strong However, Darwinius and other adapiforms fossil primates from Africa and Eurasia support for either Haplorhini or Prosimii share derived features with extant have reignited interest in the origins of (1). However, genetic markers called strepsirrhines and lack derived features Anthropoidea—monkeys, apes, and hu- short interspersed elements (SINEs) offer shared by extant tarsiers and anthropoids mans. Fossil discoveries are expanding our strong evidence in support of both – understanding of the diversity and bio- haplorhine and strepsirrhine monophyly. (6, 11 15). geography of this clade. Developments in SINEs are short segments of DNA that Several hypotheses about tarsier and molecular phylogenetics are establishing insert into the genome at apparently anthropoid origins have been proposed. a phylogenetic framework of living pri- random positions and are excellent Some researchers argue that anthropoids mates against which hypotheses about re- phylogenetic markers with an extraor- and tarsiers share a common ancestor lationships of fossils can be tested. dinarily low probability of convergent within a paraphyletic Omomyiformes Advances in genomics and the study of evolution (2). Because there are billions of whereas others assert that only tarsiers living primate ecology are enabling us to potential insertion sites in any primate have omomyiform ancestry. An alternative understand key adaptive changes in an- genome, the probability of a SINE hypothesis that we favor is that the tarsier- thropoid evolution and have reframed inserting precisely in the same locus in two anthropoid clade is the sister group of many of our adaptive questions about separate evolutionary lineages is omomyiforms as a whole. This last option human origins in the context of deep time. “exceedingly minute, and for all practical is supported by a comprehensive Here we review recent fossil discoveries, purposes, can be ignored” (p. 151, ref. 3). phylogenetic analysis (11). The developments in the study of the sensory Five SINEs support haplorhine mono- hypothetical common ancestor of tarsiers, ecology and neurobiology of anthropoids, phyly to the exclusion of strepsirrhines and anthropoids, and omomyiforms has yet to and implications from genetic research eight are shared among strepsirrhines (4). be identified, but must predate the oldest that bear on the study of Thus, the haplorhine–strepsirrhine split omomyiform, Teilhardina, from the anthropoid origins. may now be regarded as fact and must earliest Eocene of North America, underlie any phylogenetic reconstruction Europe, and Asia (16). Phylogenetics of Crown Primates of fossil primates. In the past, separate origins were Identification of which taxa of early considered for the two living clades of primates are haplorhines and which are Author contributions: B.A.W., R.F.K., and E.C.K. analyzed anthropoid primates: the New World strepsirrhines is an ongoing challenge data and B.A.W., R.F.K., and E.C.K. wrote the paper. platyrrhines and the Old World because homoplasy is common, the The authors declare no conflict of interest. catarrhines. Today, Anthropoidea is evolutionary acquisition of diagnostic This article is a PNAS Direct Submission. accepted universally as a monophyletic haplorhine and anthropoid characters 1To whom correspondence should be addressed. E-mail: group. The monophyly of the strepsirrhine occurred in mosaic fashion, and the [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.0908320107 PNAS Early Edition | 1of8 Downloaded by guest on September 30, 2021 What Is an Anthropoid? features found in living anthropoids, as have given rise to catarrhines, platyrrhines, By definition, crown Anthropoidea includes discussed below. We do not know the both, or neither (13). all species, living and fossil, descended character states for many of the presumed Propliopithecids (Aegyptopithecus and from the last common ancestor of extant Eocene anthropoids from Asia because Propliopithecus) are widely accepted as the anthropoids. Stem Anthropoidea includes they are not yet known from adequate earliest definitive representatives of the all fossil taxa that are more closely related cranial materials. Postcranial materials of catarrhine primates because of their to crown anthropoids than they are to putative Asian stem anthropoids have been dental formula (two premolars) and tarsiers, but are outside the anthropoid found in isolation, complicating their details of molar anatomy greatly fi crown group. Crown anthropoids share a speci c attribution. resembling early Miocene catarrhines number of important features. On the from east Africa (37). Oligopithecids may basis of evidence from comprehensive Anthropoid Fossils and be catarrhines. They retain some primitive phylogenetic analyses (11, 13, 17, 18), Revised Dates characteristics (small brain and unfused many of these features are considered Afro-Arabian Anthropoids. In the past mandibular symphysis), yet the dental synapomorphies. Four peculiarities of decade, finds of fossil primates have formula, large ascending process of the embryonic implantation have been augmented our picture of early premaxilla, and several features of the described (19). Extant anthropoids share talus, humerus, and femur all support anthropoids and broadened the fi 27 Alu-SINE markers (4). Most biogeographic focus of studies of catarrhine af nities (33). anthropoids have orbits that are relatively anthropoid origins (Fig. 1 and Fig. 2). Other poorly known African Paleogene small, forward facing, and convergent (20). Early anthropoids are best known from primates may be anthropoids. Altiatlasius A bony lamina posterior to the orbit the phylogenetically diverse faunas of (late Paleocene, Morocco) was described completely separates the eyes from the Afro-Arabia, especially those of the as an omomyiform (38) but may be a stem chewing muscles in the temporal fossa Fayum Depression in Egypt. The youngest anthropoid (11, 38, 39) or a stem (21). A number of other soft-tissue of the Fayum primate-bearing deposits euprimate (40). Afrotarsius, from the features of the visual system (e.g., an all- date to the Oligocene, ∼30 Ma, whereas Egyptian Oligocene, resembles stem cone retinal fovea) are anthropoid the oldest are late